International Journal of Mycobacteriology 1 (2012) 165– 169

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Review Epidemiology of cervico-facial pediatric lymphadenitis as a result of nontuberculous mycobacteria

Enrico Tortoli *

Emerging Bacterial Pathogens Unit, San Gabriele Building, San Raffaele Scientific Institute, Via Olgettina 58, 20132 Milano, Italy

ARTICLE INFO ABSTRACT

Article history: Cervical lymphadenitis as a result of nontuberculous mycobacteria, otherwise known as Received 13 October 2012 scrofula, is a disease occurring almost exclusively in immunocompetent young children. Accepted 29 October 2012 The most frequent mycobacterial species responsible is avium, but a large Available online 20 November 2012 number of other species may also be involved. The epidemiology of such disease is revised here, and the impact of different species as causative agents of adenitis is also discussed. Keywords: 2012 Asian-African Society for Mycobacteriology. All rights reserved. Cervical lymphadenitis Nontuberculous mycobacteria Epidemiology M. avium M. haemophilum M. malmoense

Contents

Introduction ...... 166 Clinical notes ...... 166 Epidemiology ...... 166 Mycobacterium scrofulaceum...... 166 MAC...... 166 complex...... 167 Mycobacterium haemophilum ...... 167 Other slowly growing species ...... 167 Rapidly growing species ...... 167 Discussion ...... 167 References ...... 168

* Tel.: +39 3292422105; fax +39 0226435183. E-mail address: [email protected]. 2212-5531/$ - see front matter 2012 Asian-African Society for Mycobacteriology. All rights reserved. http://dx.doi.org/10.1016/j.ijmyco.2012.10.008 166 International Journal of Mycobacteriology 1 (2012) 165– 169

Introduction mercialization of sensitins, despite the regret of some pedia- tricians, confirms their limited value. Scrofula is a mycobacterial disease of the lymph nodes of the The most resolutive intervention is nowadays considered head and neck well known during ancient times; in the Mid- the complete excision of the affected lymph nodes before dle Ages, it was also called the ‘‘king’s evil,’’ as it was believed the suppuration occurrence; the healing is obtained in a large the disease could be healed by the touch of royalty. Both proportion of cases, but recurrences are not exceptional. tuberculous and nontuberculous mycobacteria (NTM) can be Other less usual possibilities include no intervention, antimi- responsible for cervical lymphadenitis. crobial therapy alone, fine needle aspiration and incision fol- The cases of scrofula, which were very common in the lowed by drainage or curettage. past, are, at least in the great majority, imputable to Mycobac- terium and ; in the xx century Epidemiology this kind of disease has steadily decreased and is now very rare in developed countries, but, starting with the 1950s, an Differently from NTMs isolated from pulmonary specimens – increasing number of cases as a result of NTMs have been re- which only in a limited number of cases are clinically signif- ported [1]. icant – the mycobacteria isolated from lymph nodes can Scrofula is typically a disease of childhood, but rare cases never be considered contaminants or colonizers. The number in adults have also been documented. The focus of this review of NTM species responsible for cervical lymphadenopathy is is on the epidemiology of cervical lymphadenitis of otherwise very high, and so far some of them have only been isolated healthy children, with the exclusion therefore of cases affect- from lymph nodal biopsies. ing immunocompromised patients. Mycobacterium scrofulaceum Clinical notes M. scrofulaceum is one of the oldest of the NTM species; it was The disease typically affects immunocompetent children, described in 1956 by Prissick and Masson in a report concern- most prevalent in those between the ages of 1 and 5 years ing ten cases of a new variant of scrofula presenting with a old. It is hypothesized that NTMs present in the environment nontuberculous etiology [2]. Major emphasis is placed in this are ingested and enter the body through lesions in the oral paper on the slow growth and the yellow pigmentation of the mucosa (e.g. in concomitance with dental eruption), or by newly detected mycobacterium. The vagueness of such fea- way of the lymphatic vessels that drain the mouth and phar- tures, compatible with many mycobacterial species, were, ynx. The lymph nodes most commonly affected include the along with the name ‘‘scrofulaceum’’, destined to influence jugulodigastric, submandibular, parotid/pre-auricular, sub- the identification of mycobacteria isolated from adenitis over mental and posterior triangle. In most of the cases, the pa- a long period of time. tient is asymptomatic; less frequent symptoms can include Beginning in the 1970s, Wolinsky [3] reported an ‘‘abrupt a slight fever and malaise. The first manifestation is a non- change in the predominant etiologic agent from M. scrofulaceum tender, indolent, mostly unilateral swelling (1–6 cm) which to Mycobacterium avium complex’’ (MAC). Both the prevalent subsequently enlarges and, in consequence of the necrosis involvement of MAC and the paucity of cases due to of the central part of the granulomatous lesions, liquefies M. scrofulaceum remain unchanged nowadays. becoming fluctuant. The skin becomes often violaceous as a consequence of the inflammatory reaction, and frequently MAC the necrotic collection fistulizes. In a limited number of cases, spontaneous healing occurs The first case of cervical lymphadenitis due to M. avium was by fibrosis and calcification; regression is quite rare. reported in 1959 [4]; in subsequent years, when the taxonomic The initial stages of the disease are frequently interpreted status of MAC was still far from being defined and related as an incidental upper respiratory tract infection and antibi- organisms were referred to as ‘‘Battey group’’, the first case otics are prescribed which, however, prove to be ineffective. series were published [5,6]. Starting in the 1980s, Mycobacte- Differential diagnosis with tuberculous or pyogenic adenitis rium intracellulare was also beginning to be reported among is needed, and the isolation of the agent in a culture is of par- the agents of lymphadenitis. It remains, however, undistin- amount importance. For this purpose, the use of a liquid med- guished from M. avium of which it is considered a variant ia is advisable to reduce the burden of cases with positive [7]. The introduction of serotyping made for the first time pos- acid-fast microscopy which fails to grow if cultured on solid sible a reliable distinction between M. avium and M. intracellu- media only. lare, but, at the same time, produced the ambiguity of the The skin test based on intradermal inoculation of sensi- association of such species with M. scrofulaceum, in the M. avi- tins, tuberculin analogs specific from the most common um-intracellulare-scrofulaceum (MAIS) group [8]. With the com- NTMs, has been used for many years to diagnose, in absence mercialization of the nucleic acid probes, the definitive of a culture, NTM lymphadenitis; the diagnostic accuracy of distinction of M. avium and M. intracellulare became within such tests is at least questionable because of the high level the reach of diagnostic laboratories. of cross-reactions between the different antigens and with Recently, a large-scale study [9] did not detect any case due the tuberculin skin test itself. The discontinuation of com- to M. intracellulare in a group of children with adenitis. The International Journal of Mycobacteriology 1 (2012) 165– 169 167

same study demonstrated furthermore that all the strains of Mycobacterium mantenii [36], Mycobacterium palustre [26], Myco- M. avium investigated belonged to the subspecies hominissuis, bacterium tusciae [37] and [38]. In most with M. avium subsp. avium being totally absent. cases, such strains were included among the ones character- In recent years, MAC has been enriched by several new ized for the description of the new species. Mycobacterium species; of them, only Mycobacterium colombiense has been re- bohemicum, an uncommon mycobacterium indeed, has been ported responsible for lymphadenitis [10,11]. reported responsible for a relatively high number of cases of scrofula [39]. Mycobacterium simiae complex Mycobacterium gordonae and the members of the Mycobacte- rium terrae complex are only exceptionally responsible for dis- M. simiae, grown for the first time from a monkey, is a multi- ease in humans. Such characteristic is apparently confirmed drug-resistant species frequently isolated in several geo- for adenitis since for the first species, there is only one report graphic areas, in particular South-Western USA, Cuba and present in literature [40], and only two cases – one due to Israel. It is therefore not surprising that the involvement of [41] and one to this species in cases of adenitis has been reported right in [42] – are reported so far for the M. terrae complex. these countries [12,13]. A number of species, genetically related to M. simiae,have Rapidly growing species been described in recent years; many of them have been re- ported responsible for scrofula. Mycobacterium genavense,a The numerous cases reported above – all related to slowly species well known for its inability to grow on conventional growing species – clearly contrast with the paucity of cases solid media and for the high number of disseminated infec- imputable to rapid growers. Their isolation from cervico-fa- tions in severely immunocompromised AIDS patient, is one cial lymphadenitis is extremely rare and limited to the three of them [14]. Mycobacterium interjectum was first described fol- most common species: , Mycobacte- lowing the isolation from a lymph nodal infection in a child rium chelonae [43] and [44]. [15], and many other isolates have been reported thereafter [16–18]. Two of the strains on which is based the description of Mycobacterium triplex [19] had been grown from lymph Discussion nodes. Particularly high is the number of cases reported so far related to Mycobacterium lentiflavum [20–24]. The papers The epidemiologic picture emerging from this review is not describing the species Mycobacterium heidelbergense [25], Myco- exempt from the following biases: bacterium palustre [26], Mycobacterium parmense [27], Mycobacte- rium florentinum [28] and Mycobacterium europaeum [29] all • The high proportion of cases of M. scrofulaceum reported include one isolation from chronic pediatric until the 1980s is at least in part questionable: a number lymphadenopathy. of species, among which M. lentiflavum, M. tusciae, M. bohemicum and many others, fit the rough characteristics Mycobacterium haemophilum taken into account initially to characterize M. scrofulaceum. Furthermore, the term ‘‘scrofulaceum’’ itself may well Despite M. haemophilum is a fastidious organism which is of- have played a role in the direct assignment of such species ten missed in culture because of the requirement of particular of many of the slow growers isolated growth supplements and lower incubation temperatures, the from cases of scrofula. number of pediatric lymphadenitis due to this organism is • The use of biochemical tests, widespread until the end of quite high. A very recent review [30] reports a particularly the last century, leads to wrongly assigning all the less fre- high frequency in Israel and The Netherlands where the M. quently encountered NTMs to just one of the species (usu- haemophilum is the second most frequent organism responsi- ally no more than about 30) present in the identification ble for such disease after M. avium. In a Dutch study [31] infec- tables available in microbiological manuals. tions due to M. haemophilum, different from those due to M. • Even the use of more recent and more accurate methods avium, are associated with the involvement of multiple lymph like nucleic-acid probes is not exempt from the incorrect nodes and extranodal areas. identifications due to cross-reactivity of some of the probes (Table 1). Other slowly growing species • The lack of expertise may also lead to incorrect identifica- tion even by the users of genetic sequencing once dat- is one of the species more frequently abases that are not exhaustive or are not controlled are isolated from cervical lymphadenitis [32]; in countries where used [45]. this organism is endemic, mainly the United Kingdom and Sweden, it ranks second after M. avium. Similar is the case of It seems, therefore, not rash to assert that the role of M. Mycobacterium kansasii, which in a recent paper [33] is reported scrofulaceum is - in literature related to pediatric cervical to account for 5% of pediatric cervico-facial adenitis; more rare lymphadenitis – highly overestimated while, in contrast, is are the cases due to Mycobacterium celatum [34,35]. underestimated the involvement of many of the species de- Among the species rarely isolated in clinical laboratories, scribed in the last 20 years. at least one isolation from cervical lymphadenitis is reported It is now generally accepted that NTM species differ in for each of the following: Mycobacterium heidelbergense [25], their ability to cause lung disease in humans [46,47]. While 168 International Journal of Mycobacteriology 1 (2012) 165– 169

Table 1 – Species whose prevalence in cervical lymphadenitis is underestimated because of cross-reactions of commercial nucleic-acid probes [48] (only the species isolated at least once from cervical lymphadenitis are included).

Species Misidentifications due to cross-reactions of AccuProbea INNO LiPA mycobacteriab Genotype mycobacterium CM

M. colombiense M. intracellulare M. heidelbergense MAIS M. mantenii MAIS M. intracellulare M. nebraskense MAC or M. intracellulare M. intracellulare M. palustre MAC M. parascrofulaceum M. scrofulaceum M. scrofulaceum M. sherrisii M. simiae M. simiae a MAC, M. avium complex. b MAIS, M. avium-intracellulare-scrofulaceum group.

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